Ahead of Print -Comparison of Imported Plasmodium ovale curtisi and P. ovale wallikeri Infections among Patients in Spain, 2005–2011 - Volume 20, Number 3—March 2014 - Emerging Infectious Disease journal - CDC
Volume 20, Number 3—March 2014
Research
Comparison of Imported Plasmodium ovale curtisi and P. ovale wallikeri Infections among Patients in Spain, 2005–2011
Article Contents
Gerardo Rojo-Marcos , José Miguel Rubio-Muñoz, Germán Ramírez-Olivencia, Silvia García-Bujalance, Rosa Elcuaz-Romano, Marta Díaz-Menéndez, María Calderón, Isabel García-Bermejo, José Manuel Ruiz-Giardín, Francisco Jesús Merino-Fernández, Diego Torrús-Tendero, Alberto Delgado-Iribarren, Mónica Ribell-Bachs, Juan Arévalo-Serrano, and Juan Cuadros-González
Author affiliations: Príncipe de Asturias University Hospital, Madrid, Spain (G. Rojo-Marcos, J. Arévalo-Serrano, J. Cuadros-González,);Instituto de Salud Carlos III, Madrid (J.M. Rubio-Muñoz); Carlos III Hospital, Madrid (G. Ramírez-Olivencia); La Paz University Hospital, Madrid (S García-Bujalance); Doctor Negrín University Hospital, Las Palmas de Gran Canaria, Spain (R. Elcuaz-Romano);Ramón y Cajal Hospital, Madrid (M. Díaz-Menéndez); Gregorio Marañón University Hospital, Madrid (M. Calderón); Getafe University Hospital, Madrid (I. García-Bermejo); University Hospital of Fuenlabrada, Madrid (J. M. Ruiz-Giardín); Severo Ochoa University Hospital, Madrid (F.J. Merino-Fernández); University General Hospital of Alicante, Alicante, Spain (D. Torrús-Tendero);University Hospital Fundación Alcorcón, Madrid (A. Delgado-Iribarren); Hospital General de Granollers, Barcelona, Spain (M. Ribell-Bachs).
Abstract
Sequencing data from Plasmodium ovale genotypes co-circulating in multiple countries support the hypothesis that P. ovale curtisi and P. ovale wallikeri are 2 separate species. We conducted a multicenter, retrospective, comparative study in Spain of 21 patients who had imported P. ovale curtisi infections and 14 who had imported P. ovale wallikeri infections confirmed by PCR and gene sequencing during June 2005–December 2011. The only significant finding was more severe thrombocytopenia among patients with P. ovale wallikeriinfection than among those with P. ovale curtisi infection (p = 0.031). However, we also found nonsignificant trends showing that patients with P. ovale wallikeri infection had shorter time from arrival in Spain to onset of symptoms, lower level of albumin, higher median maximum core temperature, and more markers of hemolysis than did those with P. ovale curtisi infection. Larger, prospective studies are needed to confirm these findings.
Malaria caused by Plasmodium ovale infection has been considered a low-prevalence disease with limited geographic distribution, benign clinical course, and easy treatment; therefore, little attention has been paid to it. Diagnosis of P. ovale malaria can be difficult because of low parasitemia levels, mixed infections with other Plasmodium species, and false negatives from malaria rapid diagnostic tests (RDTs) (1). However, recent epidemiologic studies conducted by using PCR techniques have found P. ovale infections in most of sub-Saharan Africa, Southeast Asia, and the Indian subcontinent (2–5), including prevalence as high as 15% according to results of cross-sectional studies conducted in rural Nigeria (6) and Papua New Guinea (7). In addition, severe complications such as spleen rupture, severe anemia, or acute respiratory distress syndrome (ADRS) (8) may occur in patients with P. ovale malaria. Thus, the global burden of P. ovale infection might have been underestimated.
On the basis of differences in its gene sequences, P. ovale is considered to be dimorphic or to comprise 2 subspecies (2,3,9,10). This difference has hampered molecular diagnosis in some cases because of lack of DNA amplification by PCR with gene-specific primers for the small subunit ribosomal RNA (ssrRNA) (10). These subspecies had been named classic and variant P. ovale, but a comprehensive study recently described differences between these subspecies in at least 6 genes (4). These findings demonstrate that P. ovale actually consists of 2 subspecies that co-circulate in Africa and Asia and that are unable to recombine genetically; the differences seem to be explained by real biological factors, rather than ecologic or geographic factors (11).P. ovale curtisi and P. ovale wallikeri were the names proposed for these species (4).
Scant information is available on differences in clinical and analytical features, relapse profile, or accuracy of RDT results between these proposed species. Relatively high parasitemia levels were found in some patients with P. ovale wallikeri infection in Thailand (12), Vietnam (13), and Flores Island (14). A study published from a disease-endemic area of Bangladesh reported on the clinical features and degree of parasitemia in 13 patients with P. ovale wallikeri infection and 10 with P. ovale curtisi infection (5). These infections were diagnosed by PCR; only 4 of the 23 patients were symptomatic. Another recent study compared parasitemia levels, RDT results, and patient country of origin for 31 patients from Côte d’Ivoire and the Comoros Islands with imported P. ovale wallikeri infection and 59 with P. ovale curtisi infection, but no clinical data were provided (15). Clearly, information on these infections is limited.
Growth in international travel and migration has increased the incidence of imported malaria in industrialized countries. P. ovale infection may represent up to 8% of imported malaria cases, according to some published series of patients primarily from West Africa (16,17), where the proportion of sub-Saharan immigrants is high and PCR has been systematically performed. Yet, it is difficult to gather a substantial number of cases with clinico-epidemiologic correlation and molecular data. To identify clinical or analytical differences between P. ovale wallikeri and P. ovale curtisi infections and expand data on these infections, we conducted a multicenter, retrospective, comparative study of imported P. ovale infections diagnosed in Spain during 2005–2011.
Acknowledgment
We thank Francisco Javier Vilar Izquierdo for his assistance in the translation and critical review of this manuscript.
References
- Mueller I, Zimmerman PA, Reeder JC. Plasmodium malariae and Plasmodium ovale—the “bashful” malaria parasites. Trends Parasitol. 2007;23:278–83. DOIPubMed
- Tachibana M, Tsuboi T, Kaneko O, Khuntirat B, Torii M. Two types of Plasmodium ovaledefined by SSU rRNA have distinct sequences for ookinete surface proteins. Mol Biochem Parasitol. 2002;122:223–6. DOIPubMed
- Win TT, Jalloh A, Tantular IS, Tsuboi T, Ferreira MU, Kimura M, Molecular analysis ofPlasmodium ovale variants. Emerg Infect Dis. 2004;10:1235–40 . DOIPubMed
- Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Two non-recombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. J Infect Dis. 2010;201:1544–50 . DOIPubMed
- Fuehrer H-P, Habler VE, Fally MA, Harl J, Starzengruber P, Swoboda P, Plasmodium ovalein Bangladesh: genetic diversity and the first known evidence of the sympatric distribution of Plasmodium ovale curtisi and Plasmodium ovale wallikeri in southern Asia.Int J Parasitol. 2012;42:693–9 . DOIPubMed
- May J, Mockenhaupt FP, Ademowo OG, Falusi AG, Olumese PE, Bienzle U, High rate of mixed and subpatent malarial infections in southwest Nigeria. Am J Trop Med Hyg.1999;61:339–43 .PubMed
- Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg.2000;62:225–31 .PubMed
- Rojo-Marcos G, Cuadros-González J, Mesa-Latorre JM, Culebras-López AM, de Pablo-Sánchez R. Acute respiratory distress syndrome in a case of Plasmodium ovale malaria.Am J Trop Med Hyg. 2008;79:391–3 .PubMed
- Li J, Wirtz RA, McConkey GA, Sattabongkot J, Waters AP, Rogers MJ, Plasmodium: genus-conserved primers for species identification and quantitation. Exp Parasitol.1995;81:182–90. DOIPubMed
- Calderaro A, Piccolo G, Perandin F, Gorrini C, Peruzzi S, Zuelli C, Genetic polymorphisms influence Plasmodium ovale PCR detection accuracy. J Clin Microbiol. 2007;45:1624–7 . DOIPubMed
- Oguike MC, Betson M, Burke M, Nolder D, Stothard JR, Kleinschmidt I, Plasmodium ovale curtisi and Plasmodium ovale wallikeri circulate simultaneously in African communities. Int J Parasitol. 2011;41:677–83 . DOIPubMed
- Win TT, Lin K, Mizuno S, Zhou M, Liu Q, Ferreira MU, Wide distribution of Plasmodium ovale in Myanmar. Trop Med Int Health. 2002;7:231–9. DOIPubMed
- Kawamoto F, Miyake H, Kaneko O, Kimura M, Nguyen TD, Nguyen TD, Sequence variation in the 18S rRNA gene, a target for PCR-based malaria diagnosis in Plasmodium ovale from southern Vietnam. J Clin Microbiol. 1996;34:2287–9 .PubMed
- Win TT, Tantular IS, Pusarawati S, Kerong H, Lin K, Matsuoka H, Detection of Plasmodium ovale by the ICT Malaria P.f/P.v. immunochromatographic test. Acta Trop.2001;80:283–4. DOIPubMed
- Bauffe F, Desplans J, Fraisier C, Parzy D. Real-time PCR assay for discrimination ofPlasmodium ovale curtisi and Plasmodium ovale wallikeri in the Ivory Coast and in the Comoros Islands. Malar J. 2012;11:307 . DOIPubMed
- Rojo-Marcos G, Cuadros-González J, Gete-García L, Prieto-Ríos B, Arcos-Pereda P.Imported malaria in a general hospital in Madrid [in Spanish.]. Enferm Infecc Microbiol Clin. 2007;25:168–71. DOIPubMed
- Calderaro A, Gorrini C, Peruzzi S, Piccolo G, Dettori G, Chezzi C. An 8-year survey on the occurrence of imported malaria in a nonendemic area by microscopy and molecular assays. Diagn Microbiol Infect Dis. 2008;61:434–9. DOIPubMed
- Rubio JM, Post RJ, van Leeuwen WM, Henry MC, Lindergard G, Hommel M. Alternative polymerase chain reaction method to identify Plasmodium species in human blood samples: the seminested multiplex malaria PCR (SnM-PCR). Trans R Soc Trop Med Hyg.2002;96(Suppl 1):S199–204 . DOIPubMed
- World Health Organization. Severe and complicated malaria. Trans R Soc Trop Med Hyg.1990;84(Suppl 2):1–65 . DOIPubMed
- Nolder D, Oguike MC, Maxwell-Scott H, Niyazi HA, Smith V, Chiodini PL, An observational study of malaria in British travellers: Plasmodium ovale wallikeri and Plasmodium ovale curtisi differ significantly in the duration of latency. BMJ Open. 2013;3:e002711.
- Faye FB, Spiegel A, Tall A, Sokhna C, Fontenille D, Rogier C, Diagnostic criteria and risk factors for Plasmodium ovale malaria. J Infect Dis. 2002;186:690–5. DOIPubMed
- Rojo-Marcos G, Cuadros-González J, Gete-García L, Gómez-Herruz P, López-Rubio M,Esteban-Gutierrez G. Plasmodium ovale infection: description of 16 cases and a review[in Spanish.]. Enferm Infecc Microbiol Clin. 2011;29:204–8 . DOIPubMed
- Kawamoto F, Liu Q, Ferreira MU, Tantular IS. How prevalent are Plasmodium ovale and P. malariae in East Asia? Parasitol Today. 1999;15:422–6 . DOIPubMed
- Bruce MC, Macheso A, Kelly-Hope LA, Nkhoma S, McConnachie A, Molyneux ME. Effect of transmission setting and mixed species infections on clinical measures of malaria in Malawi. PLoS ONE. 2008;3:e2775 . DOIPubMed
- Lacerda MV, Mourão MP, Coelho HC, Santos JB. Thrombocytopenia in malaria: who cares? Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):52–63 . DOIPubMed
- Saravu K, Docherla M, Vasudev A, Shastry BA. Thrombocytopenia in vivax and falciparum malaria: an observational study of 131 patients in Karnataka, India. Ann Trop Med Parasitol. 2011;105:593–8 . DOIPubMed
- Moody A. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev. 2002;15:66–78. DOIPubMed
- Bigaillon C, Fontan E, Cavallo JD, Hernandez E, Spiegel A. Ineffectiveness of the Binax NOW malaria test for diagnosis of Plasmodium ovale malaria. J Clin Microbiol.2005;43:1011 . DOIPubMed
- Fançony C, Gamboa D, Sebastião Y, Hallett R, Sutherland C, Sousa-Figueiredo JC,Various pfcrt and pfmdr1 genotypes of Plasmodium falciparum cocirculate with P. malariae, P. ovale spp., and P. vivax in northern Angola. Antimicrob Agents Chemother.2012;56:5271–7 . DOIPubMed
- Danquah I, Bedu-Addo G, Mockenhaupt FP. Type 2 diabetes mellitus and increased risk for malaria infection. Emerg Infect Dis. 2010;16:1601–4 . DOIPubMed
Tables
- Table 1. Demographic and epidemiologic characteristics of patients with imported Plasmodium ovale curtisi or P. ovale wallikeri infections, Spain, 2005–2011
- Table 2. Microbiological characteristics of patients with imported Plasmodium ovale curtisi or P. ovale wallikeri infections, Spain, 2005–2011
- Table 3. Clinical and therapeutic characteristics of patients with imported Plasmodium ovale curtisi or P. ovale wallikeri infections, Spain, 2005–2011
Suggested citation for this article: Rojo-Marcos G, Rubio-Muñoz JM, Ramírez-Olivencia G, García-Bujalance S, Elcuaz-Romano R, Díaz-Menéndez M, et al. Comparison of imported Plasmodium ovale curtisi and P. ovale wallikeri infections among patients in Spain, 2005–2011. Emerg Infect Dis [Internet]. 2014 Mar [date cited]. http://dx.doi.org/10.3201/eid2003.130745
DOI: 10.3201/eid2003.130745
No hay comentarios:
Publicar un comentario